A voltage-dependent chloride channel fine-tunes photosynthesis in plants

Abstract

In natural habitats, plants frequently experience rapid changes in the intensity of sunlight. To cope with these changes and maximize growth, plants adjust photosynthetic light utilization in electron transport and photoprotective mechanisms. This involves a proton motive force (PMF) across the thylakoid membrane, postulated to be affected by unknown anion (Cl−) channels. Here we report that a bestrophin-like protein from Arabidopsis thaliana functions as a voltage-dependent Cl− channel in electrophysiological experiments. AtVCCN1 localizes to the thylakoid membrane, and fine-tunes PMF by anion influx into the lumen during illumination, adjusting electron transport and the photoprotective mechanisms. The activity of AtVCCN1 accelerates the activation of photoprotective mechanisms on sudden shifts to high light. Our results reveal that AtVCCN1, a member of a conserved anion channel family, acts as an early component in the rapid adjustment of photosynthesis in variable light environments.

A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments

“…S13 and S14) suggests that NPQ deficiency does not have a deleterious effect on plant vegetative growth acclimation under long-term fluctuating light conditions. In contrast, NPQ was demonstrated to play a crucial role in rapid adjustments of photosynthesis to artificial fluctuating light and shading (49)(50)(51)(52). Although npq mutants suffered higher photoinhibition and had less seeds relative to the wild type in field experiments, they did not display visible vegetative growth defects (53,54).…”

Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH

“…In any case, the balancing of Δψ/ΔpH, and its kinetics, are dependent on the regulation of counter-ion homeostasis in the chloroplast (34), and recent work from several labs has identified putative components of these ion homeostatic machineries, including a thylakoid potassium channel (35), a K + /H + antiporter (36), as well as transporters for other charged species (37)(38)(39)(40)(41). There are also indications that the Δψ/ΔpH balance is controlled by the synthesis of membrane permeable weak bases, such as putrescene, that effectively increase the proton buffering capacity of the lumen (42).…”

Dynamic photosynthesis under a fluctuating environment: a modelling-based analysis

“…Recent experimental evidence indicates that the partitioning of pmf into its pH and electrical components is regulated by the activities of such channels (Armbruster et al, 2014;Kunz et al, 2014;Herdean et al, 2016). However, quantitative information of the kinetics and regulation of these channels is still lacking which prevents the development of a mechanistic model.…”

“…From the data reported by Herdean et al (2016) and , three photosynthetic induction curves from darkness to 70 μmol m −2 s −1 , 600 μmol m −2 s −1 and 1000 μmol m −2 s −1 were chosen, all measured at ambient CO2, and O2. The simulation protocol was adapted to the experimental conditions and flashes were simulated at the same timepoints as in the experiments and with the same flash intensities.…”

“…Given the large uncertainty in XGL ∫ƒ values from different sources and the fact that the model does not take into account the effect of photoinhibition, XGL ∫ƒ simulations were tested only with measurements by and Herdean et al (2016) for the first 10 minutes after an increase in irradiance from a dark adapted state, assuming that, under such conditions, XGL ∫ƒ is mostly determined by the qE mechanism and chloroplast movement. The same experiments were also used to test dynamic simulations of .…”